P2X2 Receptor Expression and Function Is Upregulated in the Rat Supraoptic Nucleus Stimulated Through Refeeding After Fasting

. 2019 ; 13 () : 284. [epub] 20190626

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31297050

Magnocellular neurons in the supraoptic nucleus (SON), which synthesize and release arginine vasopressin (AVP) and oxytocin (OT), express several subtypes of ATP-stimulated purinergic P2X receptors (P2XR) that modulate neuronal activity as well as neurotransmitter and hormone release. However, the physiological impact of this modulation is not well understood. Here, we tested a hypothesis that P2XRs play a role in the sustained release of hormones from SON neurons stimulated through fasting/refeeding. We studied the effect of 2 h of refeeding after 48 h of fasting on P2XR and P2YR mRNA expression and ATP-induced presynaptic and postsynaptic responses in the SON of 30-day-old rats. Quantitative real-time PCR revealed that the expression of P2X2R and AVP mRNA was upregulated, whereas P2X4R, P2X7R, P2Y2R, and OT mRNA levels were not significantly changed and P2Y1R mRNA expression was decreased. Whole-cell patch clamp recordings performed on isolated rat brain slices showed that the amplitude of the ATP-stimulated somatic current and the ATP-induced increases in the frequency of spontaneous GABAergic inhibitory postsynaptic currents were significantly higher in SON neurons from fasted/refed rats than in SON neurons from normally fed rats. No evidence was found for changes in the presynaptic effect of ATP in SON neurons not expressing somatic P2XRs. These results suggest that the increased activity of SON neurons synthesizing AVP is associated with enhanced expression of P2X2Rs on neuronal cell bodies and their GABAergic presynaptic nerve terminals.

Zobrazit více v PubMed

Armstrong W. E. (2007). The neurophysiology of neurosecretory cells. PubMed DOI PMC

Bhattacharya A., Vavra V., Svobodova I., Bendova Z., Vereb G., Zemkova H. (2013). Potentiation of inhibitory synaptic transmission by extracellular ATP in rat suprachiasmatic nuclei. PubMed DOI PMC

Bo X., Zhang Y., Nassar M., Burnstock G., Schoepfer R. (1995). A P2X purinoceptor cDNA conferring a novel pharmacological profile. PubMed DOI

Boudaba C., Di S., Tasker J. G. (2003). Presynaptic noradrenergic regulation of glutamate inputs to hypothalamic magnocellular neurones. PubMed DOI

Brussaard A. B., Kits K. S. (1999). Changes in GABAA receptor-mediated synaptic transmission in oxytocin neurons during female reproduction: plasticity in a neuroendocrine context. PubMed DOI

Burlet A. J., Jhanwar-Uniyal M., Chapleur-Chateau M., Burlet C. R., Leibowitz S. F. (1992). Effect of food deprivation and refeeding on the concentration of vasopressin and oxytocin in discrete hypothalamic sites. PubMed DOI

Burnstock G. (2006). Purinergic signalling–an overview. PubMed

Carreno F. R., Walch J. D., Dutta M., Nedungadi T. P., Cunningham J. T. (2011). Brain-derived neurotrophic factor-tyrosine kinase B pathway mediates NMDA receptor NR2B subunit phosphorylation in the supraoptic nuclei following progressive dehydration. PubMed DOI PMC

Choe K. Y., Han S. Y., Gaub P., Shell B., Voisin D. L., Knapp B. A., et al. (2015). High salt intake increases blood pressure via BDNF-mediated downregulation of KCC2 and impaired baroreflex inhibition of vasopressin neurons. PubMed DOI PMC

Collo G., North R. A., Kawashima E., Merlo-Pich E., Neidhart S., Surprenant A., et al. (1996). Cloning OF P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. PubMed DOI PMC

Custer E. E., Knott T. K., Cuadra A. E., Ortiz-Miranda S., Lemos J. R. (2012). P2X purinergic receptor knockout mice reveal endogenous ATP modulation of both vasopressin and oxytocin release from the intact neurohypophysis. PubMed DOI PMC

Day T. A., Sibbald J. R., Khanna S. (1993). ATP mediates an excitatory noradrenergic neuron input to supraoptic vasopressin cells. PubMed DOI

de Kock C. P., Burnashev N., Lodder J. C., Mansvelder H. D., Brussaard A. B. (2004). NMDA receptors induce somatodendritic secretion in hypothalamic neurones of lactating female rats. PubMed DOI PMC

Decavel C., Curras M. C. (1997). Increased expression of the N-methyl-D-aspartate receptor subunit. NR1, in immunohistochemically identified magnocellular hypothalamic neurons during dehydration. PubMed DOI

Espallergues J., Solovieva O., Técher V., Bauer K., Alonso G., Vincent A., et al. (2007). Synergistic activation of astrocytes by ATP and norepinephrine in the rat supraoptic nucleus. PubMed DOI

Gomes D. A., Song Z., Stevens W., Sladek C. D. (2009). Sustained stimulation of vasopressin and oxytocin release by ATP and phenylephrine requires recruitment of desensitization-resistant P2X purinergic receptors. PubMed DOI PMC

Gordon G. R., Iremonger K. J., Kantevari S., Ellis-Davies G. C., MacVicar B. A., Bains J. S. (2009). Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. PubMed DOI PMC

Gottlieb H. B., Ji L. L., Cunningham J. T. (2011). Role of superior laryngeal nerve and Fos staining following dehydration and rehydration in the rat. PubMed DOI PMC

Hu B., Bourque C. W. (1991). Functional N-Methyl-D-Aspartate and non-N-Methyl-D-aspartate receptors are expressed by rat supraoptic neurosecretory cells in vitro. PubMed DOI

Iremonger K. J., Benediktsson A. M., Bains J. S. (2010). Glutamatergic synaptic transmission in neuroendocrine cells: basic principles and mechanisms of plasticity. PubMed DOI

Israel J. M., Poulain D. A., Oliet S. H. (2010). Glutamatergic inputs contribute to phasic activity in vasopressin neurons. PubMed DOI PMC

Jhamandas J. H., Raby W., Rogers J., Buijs R. M., Renaud L. P. (1989). Diagonal band projection towards the hypothalamic supraoptic nucleus: light and electron microscopic observations in the rat. PubMed DOI

Johnstone L. E., Fong T. M., Leng G. (2006). Neuronal activation in the hypothalamus and brainstem during feeding in rats. PubMed DOI

Jones B. E., Moore R. Y. (1977). Ascending projections of the locus coeruleus in the rat. II. autoradiographic study. PubMed

Jourdain P., Israel J. M., Dupouy B., Oliet S. H., Allard M., Vitiello S., et al. (1998). Evidence for a hypothalamic oxytocin-sensitive pattern-generating network governing oxytocin neurons in vitro. PubMed DOI PMC

Khakh B. S., North R. A. (2012). Neuromodulation by extracellular ATP and P2X receptors in the CNS. PubMed DOI PMC

Knott T. K., Marrero H. G., Custer E. E., Lemos J. R. (2008). Endogenous ATP potentiates only vasopressin secretion from neurohypophysial terminals. PubMed DOI

Kohno D., Nakata M., Maejima Y., Shimizu H., Sedbazar U., Yoshida N., et al. (2008). Nesfatin-1 neurons in paraventricular and supraoptic nuclei of the rat hypothalamus coexpress oxytocin and vasopressin and are activated by refeeding. PubMed DOI

Kombian S. B., Hirasawa M., Mouginot D., Pittman Q. J. (2002). Modulation of synaptic transmission by oxytocin and vasopressin in the supraoptic nucleus. PubMed DOI

Lemos J. R., Custer E. E., Ortiz-Miranda S. (2018). Purinergic receptor types in the hypothalamic-neurohypophysial system. PubMed PMC

Leng G., Brown C. H., Russell J. A. (1999). Physiological pathways regulating the activity of magnocellular neurosecretory cells. PubMed DOI

Leng G., Ludwig M. (2008). Neurotransmitters and peptides: whispered secrets and public announcements. PubMed DOI PMC

Leranth C., Zaborszky L., Marton J., Palkovits M. (1975). Quantitative studies on the supraoptic nucleus in the rat. I. synaptic organization. PubMed

Li C., Tripathi P. K., Armstrong W. E. (2007). Differences in spike train variability in rat vasopressin and oxytocin neurons and their relationship to synaptic activity. PubMed DOI PMC

Loesch A., Miah S., Burnstock G. (1999). Ultrastructural localisation of ATP-gated P2X2 receptor immunoreactivity in the rat hypothalamo-neurohypophysial system. PubMed

Lucio-Oliveira F., Franci C. R. (2012). Effect of the interaction between food state and the action of estrogen on oxytocinergic system activity. PubMed DOI

Lucio-Oliveira F., Traslavina G. A., Borges B. D., Franci C. R. (2015). Modulation of the activity of vasopressinergic neurons by estrogen in rats refed with normal or sodium-free food after fasting. PubMed DOI

Ludwig M. (1998). Dendritic release of vasopressin and oxytocin. PubMed DOI

Meeker R. B., Swanson D. J., Greenwood R. S., Hayward J. N. (1993). Quantitative mapping of glutamate presynaptic terminals in the supraoptic nucleus and surrounding hypothalamus. PubMed DOI

Moos F. C. (1995). GABA-induced facilitation of the periodic bursting activity of oxytocin neurones in suckled rats. PubMed DOI PMC

Nissen R., Cunningham J. T., Renaud L. P. (1993). Lateral hypothalamic lesions alter baroreceptor-evoked inhibition of rat supraoptic vasopressin neurones. PubMed DOI PMC

Oliet S. H., Bourque C. W. (1993). Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. PubMed DOI

Panatier A., Oliet S. H. (2006). Neuron-glia interactions in the hypothalamus. PubMed DOI

Poplawski M. M., Mastaitis J. W., Yang X. J., Mobbs C. V. (2010). Hypothalamic responses to fasting indicate metabolic reprogramming away from glycolysis toward lipid oxidation. PubMed DOI PMC

Richard P., Moos F., Freund-Mercier M. J. (1991). Central effects of oxytocin. PubMed DOI

Schicker K. W., Chandaka G. K., Geier P., Kubista H., Boehm S. (2010). P2Y1 receptors mediate an activation of neuronal calcium-dependent K+ channels. PubMed DOI PMC

Shibuya I., Kabashima N., Ibrahim N., Setiadji S. V., Ueta Y., Yamashita H. (2000). Pre- and postsynaptic modulation of the electrical activity of rat supraoptic neurones. PubMed DOI

Shibuya I., Tanaka K., Hattori Y., Uezono Y., Harayama N., Noguchi J., et al. (1999). Evidence that multiple P2X purinoceptors are functionally expressed in rat supraoptic neurones. PubMed DOI PMC

Sladek C. D., Kapoor J. R. (2001). Neurotransmitter/neuropeptide interactions in the regulation of neurohypophyseal hormone release. PubMed DOI

Song Z., Sladek C. D. (2006). Site of ATP and phenylephrine synergistic stimulation of vasopressin release from the hypothalamo-neurohypophyseal system. PubMed DOI

Song Z., Vijayaraghavan S., Sladek C. D. (2007). ATP increases intracellular calcium in supraoptic neurons by activation of both P2X and P2Y purinergic receptors. PubMed

Tappaz M. L., Wassef M., Oertel W. H., Paut L., Pujol J. F. (1983). Light- and electron-microscopic immunocytochemistry of glutamic acid decarboxylase (GAD) in the basal hypothalamus: morphological evidence for neuroendocrine gamma-aminobutyrate (GABA). PubMed DOI

Theodosis D. T., Paut L., Tappaz M. L. (1986). Immunocytochemical analysis of the GABAergic innervation of oxytocin- and vasopressin-secreting neurons in the rat supraoptic nucleus. PubMed DOI

Timofeeva E., Baraboi E. D., Richard D. (2005). Contribution of the vagus nerve and lamina terminalis to brain activation induced by refeeding. PubMed DOI

Troadec J. D., Thirion S., Nicaise G., Lemos J. R., Dayanithi G. (1998). ATP-evoked increases in [Ca2+]i and peptide release from rat isolated neurohypophysial terminals via a P2X2 purinoceptor. PubMed DOI PMC

Vavra V., Bhattacharya A., Zemkova H. (2011). Facilitation of glutamate and GABA release by P2X receptor activation in supraoptic neurons from freshly isolated rat brain slices. PubMed DOI

Vilhena-Franco T., Valentim-Lima E., Reis L. C., Elias L. L. K., Antunes-Rodrigues J., Mecawi A. S. (2018). Role of AMPA and NMDA receptors on vasopressin and oxytocin secretion induced by hypertonic extracellular volume expansion. PubMed DOI

Voisin D. L., Herbison A. E., Poulain D. A. (1995). Central inhibitory effects of muscimol and bicuculline on the milk ejection reflex in the anaesthetized rat. PubMed DOI PMC

Vulchanova L., Arvidsson U., Riedl M., Wang J., Buell G., Surprenant A., et al. (1996). Differential distribution of two ATP-gated channels (P2X receptors) determined by immunocytochemistry. PubMed DOI PMC

Wang L., Ennis M., Szabo G., Armstrong W. E. (2015). Characteristics of GABAergic and cholinergic neurons in perinuclear zone of mouse supraoptic nucleus. PubMed DOI PMC

Weiss M. L., Hatton G. I. (1990). Collateral input to the paraventricular and supraoptic nuclei in rat. I. Afferents from the subfornical organ and the anteroventral third ventricle region. PubMed DOI

Wuarin J. P., Dudek F. E. (1993). Patch-clamp analysis of spontaneous synaptic currents in supraoptic neuroendocrine cells of the rat hypothalamus. PubMed DOI PMC

Xiang Z., Bo X., Oglesby I., Ford A., Burnstock G. (1998). Localization of ATP-gated P2X2 receptor immunoreactivity in the rat hypothalamus. PubMed DOI

Yao S. T., Gouraud S. S., Qiu J., Cunningham J. T., Paton J. F., Murphy D. (2012). Selective up-regulation of JunD transcript and protein expression in vasopressinergic supraoptic nucleus neurones in water-deprived rats. PubMed DOI PMC

Yoshimura M., Ohkubo J., Katoh A., Ohno M., Ishikura T., Kakuma T., et al. (2013). A c-fos-monomeric red fluorescent protein 1 fusion transgene is differentially expressed in rat forebrain and brainstem after chronic dehydration and rehydration. PubMed DOI

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Cell Type-Specific Expression of Purinergic P2X Receptors in the Hypothalamus

. 2025 May 22 ; 26 (11) : . [epub] 20250522

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...